Melatonin controls experimental autoimmune encephalomyelitis by altering the T effector/regulatory balance

Brain, Behavior, and Immunity

Volumn 50, Issue , 2015, Pages 101-114

  Álvarez Sánchez, Nuria ^a   Cruz Chamorro, Ivan ^a,b   López González, Antonio ^a   Utrilla, José C ^b   Fernández Santos, José M ^b   Martínez López, Alicia ^a,b   Lardone, Patricia J ^a,b   Guerrero, Juan M ^a,b   Carrillo Vico, Antonio ^a,b  

^a HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

^b UNIVERSITY OF SEVILLE   (Spain)

Author keywords

CD44; EAE MS; IL 10; Melatonin; T effector memory cells; T regulatory cells; Th1; Th17

Indexed keywords

HERMES ANTIGEN; INTERLEUKIN 10; MELATONIN; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; CYTOKINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; ANIMAL; C57BL MOUSE; CELL PROLIFERATION; CHEMICALLY INDUCED; DRUG EFFECTS; IMMUNOLOGY; INFLAMMATION; LYMPH NODE; METABOLISM; SPINAL CORD;

ANIMALS; CELL PROLIFERATION; CYTOKINES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; INFLAMMATION; LYMPH NODES; MELATONIN; MICE; MICE, INBRED C57BL; SPINAL CORD; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TH17 CELLS;

EID: 84934299916     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2015.06.021     Document Type: Article

References (76)

1. Akpinar Z., Tokgoz S., Gokbel H., Okudan N., Uguz F., Yilmaz G. The association of nocturnal serum melatonin levels with major depression in patients with acute multiple sclerosis. Psychiatry Res. 2008, 161:253-257.
2. Baaten B.J., Tinoco R., Chen A.T., Bradley L.M. Regulation of antigen-experienced T cells: lessons from the quintessential memory marker CD44. Front. Immunol. 2012, 3:23.
3. Bahamonde C., Conde C., Aguera E., Lillo R., Luque E., Gascon F., Feijoo M., Cruz A.H., Sanchez-Lopez F., Tunez I. Elevated melatonin levels in natalizumab-treated female patients with relapsing-remitting multiple sclerosis: relationship to oxidative stress. Eur. J. Pharmacol. 2014, 730:26-30.
4. Baron J.L., Madri J.A., Ruddle N.H., Hashim G., Janeway C.A. Surface expression of alpha 4 integrin by CD4 T cells is required for their entry into brain parenchyma. J. Exp. Med. 1993, 177:57-68.
5. Bollyky P.L., Lord J.D., Masewicz S.A., Evanko S.P., Buckner J.H., Wight T.N., Nepom G.T. Cutting edge: high molecular weight hyaluronan promotes the suppressive effects of CD4+CD25+ regulatory T cells. J. Immunol. 2007, 179:744-747.
6. Bollyky P.L., Falk B.A., Long S.A., Preisinger A., Braun K.R., Wu R.P., Evanko S.P., Buckner J.H., Wight T.N., Nepom G.T. CD44 costimulation promotes FoxP3+ regulatory T cell persistence and function via production of IL-2, IL-10, and TGF-beta. J. Immunol. 2009, 183:2232-2241.
7. Brocke S., Piercy C., Steinman L., Weissman I.L., Veromaa T. Antibodies to CD44 and integrin alpha4, but not L-selectin, prevent central nervous system inflammation and experimental encephalomyelitis by blocking secondary leukocyte recruitment. Proc. Natl. Acad. Sci. USA 1999, 96:6896-6901.
8. Cabrera J., Quintana J., Reiter R.J., Loro J., Cabrera F., Estevez F. Melatonin prevents apoptosis and enhances HSP27 mRNA expression induced by heat shock in HL-60 cells: possible involvement of the MT2 receptor. J. Pineal Res. 2003, 35:231-238.
9. Calvo J.R., Gonzalez-Yanes C., Maldonado M.D. The role of melatonin in the cells of the innate immunity: a review. J. Pineal Res. 2013, 55:103-120.
10. Carrillo-Vico A., Lardone P.J., Naji L., Fernandez-Santos J.M., Martin-Lacave I., Guerrero J.M., Calvo J.R. Beneficial pleiotropic actions of melatonin in an experimental model of septic shock in mice: regulation of pro-/anti-inflammatory cytokine network, protection against oxidative damage and anti-apoptotic effects. J. Pineal Res. 2005, 39:400-408.
11. Carrillo-Vico A., Leech M.D., Anderton S.M. Contribution of myelin autoantigen citrullination to T cell autoaggression in the central nervous system. J. Immunol. 2010, 184:2839-2846.
12. Carrillo-Vico A., Lardone P.J., Alvarez-Sanchez N., Rodriguez-Rodriguez A., Guerrero J.M. Melatonin: buffering the immune system. Int. J. Mol. Sci. 2013, 14:8638-8683.
13. Chastain E.M., Duncan D.S., Rodgers J.M., Miller S.D. The role of antigen presenting cells in multiple sclerosis. Biochim. Biophys. Acta 2011, 1812:265-274.
14. Constantinescu C.S., Hilliard B., Ventura E., Rostami A. Luzindole, a melatonin receptor antagonist, suppresses experimental autoimmune encephalomyelitis. Pathobiology 1997, 65:190-194.
15. Damasceno A., Moraes A.S., Farias A., Damasceno B.P., Dos Santos L.M., Cendes F. Disruption of melatonin circadian rhythm production is related to multiple sclerosis severity: a preliminary study. J. Neurol. Sci. 2015, 10.1016/j.jns.2015.03.040: 10.1016/j.jns.2015.1003.1040.
16. Deiss A., Brecht I., Haarmann A., Buttmann M. Treating multiple sclerosis with monoclonal antibodies: a 2013 update. Expert Rev. Neurother. 2013, 13:313-335.
17. Ding K., Wang H., Xu J., Lu X., Zhang L., Zhu L. Melatonin reduced microglial activation and alleviated neuroinflammation induced neuron degeneration in experimental traumatic brain injury: possible involvement of mTOR pathway. Neurochem. Int. 2014, 76:23-31.
18. Fillatreau S., Sweenie C.H., McGeachy M.J., Gray D., Anderton S.M. B cells regulate autoimmunity by provision of IL-10. Nat. Immunol. 2002, 3:944-950.
19. Firan M., Dhillon S., Estess P., Siegelman M.H. Suppressor activity and potency among regulatory T cells is discriminated by functionally active CD44. Blood 2006, 107:619-627.
20. Francisco L.M., Sage P.T., Sharpe A.H. The PD-1 pathway in tolerance and autoimmunity. Immunol. Rev. 2010, 236:219-242.
21. Fritzsching B., Haas J., Konig F., Kunz P., Fritzsching E., Poschl J., Krammer P.H., Bruck W., Suri-Payer E., Wildemann B. Intracerebral human regulatory T cells: analysis of CD4+ CD25+ FOXP3+ T cells in brain lesions and cerebrospinal fluid of multiple sclerosis patients. PLoS One 2011, 6:e17988.
22. Frohman E.M., Racke M.K., Raine C.S. Multiple sclerosis-the plaque and its pathogenesis. N. Engl. J. Med. 2006, 354:942-955.
23. Ghazi-Visser L., Laman J.D., Nagel S., van Meurs M., van Riel D., Tzankov A., Frank S., Adams H., Wolk K., Terracciano L., Melief M.J., Sabat R., Gunthert U. CD44 variant isoforms control experimental autoimmune encephalomyelitis by affecting the lifespan of the pathogenic T cells. FASEB J. 2013, 27:3683-3701.
24. Guan H., Nagarkatti P.S., Nagarkatti M. CD44 reciprocally regulates the differentiation of encephalitogenic Th1/Th17 and Th2/regulatory T cells through epigenetic modulation involving DNA methylation of cytokine gene promoters, thereby controlling the development of experimental autoimmune encephalomyelitis. J. Immunol. 2011, 186:6955-6964.
25. Hardeland R. Melatonin and the theories of aging: a critical appraisal of melatonin's role in antiaging mechanisms. J. Pineal Res. 2013, 55:325-356.
26. Hofman F.M., Hinton D.R., Johnson K., Merrill J.E. Tumor necrosis factor identified in multiple sclerosis brain. J. Exp. Med. 1989, 170:607-612.
27. Horwitz M.S., Evans C.F., McGavern D.B., Rodriguez M., Oldstone M.B. Primary demyelination in transgenic mice expressing interferon-gamma. Nat. Med. 1997, 3:1037-1041.
28. Jankovic B.D., Isakovic K., Petrovic S. Effect of pinealectomy on immune reactions in the rat. Immunology 1970, 18:1-6.
29. Jiang D., Liang J., Noble P.W. Hyaluronan as an immune regulator in human diseases. Physiol. Rev. 2011, 91:221-264.
30. Kang J.C., Ahn M., Kim Y.S., Moon C., Lee Y., Wie M.B., Lee Y.J., Shin T. Melatonin ameliorates autoimmune encephalomyelitis through suppression of intercellular adhesion molecule-1. J. Vet. Sci. 2001, 2:85-89.
31. Kebir H., Kreymborg K., Ifergan I., Dodelet-Devillers A., Cayrol R., Bernard M., Giuliani F., Arbour N., Becher B., Prat A. Human TH17 lymphocytes promote blood-brain barrier disruption and central nervous system inflammation. Nat. Med. 2007, 13:1173-1175.
32. Kiefer R., Schweitzer T., Jung S., Toyka K.V., Hartung H.P. Sequential expression of transforming growth factor-beta1 by T-cells, macrophages, and microglia in rat spinal cord during autoimmune inflammation. J. Neuropathol. Exp. Neurol. 1998, 57:385-395.
33. Kivisakk P., Mahad D.J., Callahan M.K., Trebst C., Tucky B., Wei T., Wu L., Baekkevold E.S., Lassmann H., Staugaitis S.M., Campbell J.J., Ransohoff R.M. Human cerebrospinal fluid central memory CD4+ T cells: evidence for trafficking through choroid plexus and meninges via P-selectin. Proc. Natl. Acad. Sci. USA 2003, 100:8389-8394.
34. Kreymborg K., Etzensperger R., Dumoutier L., Haak S., Rebollo A., Buch T., Heppner F.L., Renauld J.C., Becher B. IL-22 is expressed by Th17 cells in an IL-23-dependent fashion, but not required for the development of autoimmune encephalomyelitis. J. Immunol. 2007, 179:8098-8104.
35. Kroenke M.A., Carlson T.J., Andjelkovic A.V., Segal B.M. IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 2008, 205:1535-1541.
36. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., McClanahan T., Kastelein R.A., Cua D.J. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005, 201:233-240.
37. Lardone P.J., Guerrero J.M., Fernandez-Santos J.M., Rubio A., Martin-Lacave I., Carrillo-Vico A. Melatonin synthesized by T lymphocytes as a ligand of the retinoic acid-related orphan receptor. J. Pineal Res. 2011, 51:454-462.
38. Liu H., Xu L., Wei J.E., Xie M.R., Wang S.E., Zhou R.X. Role of CD4+ CD25+ regulatory T cells in melatonin-mediated inhibition of murine gastric cancer cell growth in vivo and in vitro. Anat. Rec. (Hoboken) 2011, 294:781-788.
39. Liu C.Y., Guo S.D., Yu J.Z., Li Y.H., Zhang H., Feng L., Chai Z., Yuan H.J., Yang W.F., Feng Q.J., Xiao B.G., Ma C.G. Fasudil mediates cell therapy of EAE by immunomodulating encephalomyelitic T cells and macrophages. Eur. J. Immunol. 2015, 45:142-152.
40. Lock C., Hermans G., Pedotti R., Brendolan A., Schadt E., Garren H., Langer-Gould A., Strober S., Cannella B., Allard J., Klonowski P., Austin A., Lad N., Kaminski N., Galli S.J., Oksenberg J.R., Raine C.S., Heller R., Steinman L. Gene-microarray analysis of multiple sclerosis lesions yields new targets validated in autoimmune encephalomyelitis. Nat. Med. 2002, 8:500-508.
41. Lopez-Gonzalez A., Alvarez-Sanchez N., Lardone P.J., Cruz-Chamorro I., Martinez-Lopez A., Guerrero J.M., Reiter R.J., Carrillo-Vico A. Melatonin treatment improves primary progressive multiple sclerosis: a case report. J. Pineal Res. 2015, 58:173-177.
42. Mao P., Manczak M., Shirendeb U.P., Reddy P.H. MitoQ, a mitochondria-targeted antioxidant, delays disease progression and alleviates pathogenesis in an experimental autoimmune encephalomyelitis mouse model of multiple sclerosis. Biochim. Biophys. Acta 2013, 1832:2322-2331.
43. Masana M.I., Doolen S., Ersahin C., Al-Ghoul W.M., Duckles S.P., Dubocovich M.L., Krause D.N. MT(2) melatonin receptors are present and functional in rat caudal artery. J. Pharmacol. Exp. Ther. 2002, 302:1295-1302.
44. Mathes A.M., Wolf B., Rensing H. Melatonin receptor antagonist luzindole is a powerful radical scavenger in vitro. J. Pineal Res. 2008, 45:337-338.
45. Mauriz J.L., Collado P.S., Veneroso C., Reiter R.J., Gonzalez-Gallego J. A review of the molecular aspects of melatonin's anti-inflammatory actions: recent insights and new perspectives. J. Pineal Res. 2013, 54:1-14.
46. McGeachy M.J., Stephens L.A., Anderton S.M. Natural recovery and protection from autoimmune encephalomyelitis: contribution of CD4+CD25+ regulatory cells within the central nervous system. J. Immunol. 2005, 175:3025-3032.
47. Medrano-Campillo P., Sarmiento-Soto H., Alvarez-Sanchez N., Alvarez-Rios A.I., Guerrero J.M., Rodriguez-Prieto I., Castillo-Palma M.J., Lardone P.J., Carrillo-Vico A. Evaluation of the immunomodulatory effect of melatonin on the T-cell response in peripheral blood from systemic lupus erythematosus patients. J. Pineal Res. 2015, 58:219-226.
48. Melamud L., Golan D., Luboshitzky R., Lavi I., Miller A. Melatonin dysregulation, sleep disturbances and fatigue in multiple sclerosis. J. Neurol. Sci. 2012, 314:37-40.
49. Merrill J.E., Kono D.H., Clayton J., Ando D.G., Hinton D.R., Hofman F.M. Inflammatory leukocytes and cytokines in the peptide-induced disease of experimental allergic encephalomyelitis in SJL and B10.PL mice. Proc. Natl. Acad. Sci. USA 1992, 89:574-578.
50. Milo R., Kahana E. Multiple sclerosis: geoepidemiology, genetics and the environment. Autoimmun. Rev. 2010, 9:A387-394.
51. Mizuno T., Zhang G., Takeuchi H., Kawanokuchi J., Wang J., Sonobe Y., Jin S., Takada N., Komatsu Y., Suzumura A. Interferon-gamma directly induces neurotoxicity through a neuron specific, calcium-permeable complex of IFN-gamma receptor and AMPA GluR1 receptor. FASEB J. 2008, 22:1797-1806.
52. Natarajan R., Einarsdottir E., Riutta A., Hagman S., Raunio M., Mononen N., Lehtimaki T., Elovaara I. Melatonin pathway genes are associated with progressive subtypes and disability status in multiple sclerosis among Finnish patients. J. Neuroimmunol. 2012, 250:106-110.
53. Negi G., Kumar A., Sharma S.S. Melatonin modulates neuroinflammation and oxidative stress in experimental diabetic neuropathy: effects on NF-kappaB and Nrf2 cascades. J. Pineal Res. 2011, 50:124-131.
54. Panitch H.S., Hirsch R.L., Haley A.S., Johnson K.P. Exacerbations of multiple sclerosis in patients treated with gamma interferon. Lancet 1987, 1:893-895.
55. Pouly S., Becher B., Blain M., Antel J.P. Interferon-gamma modulates human oligodendrocyte susceptibility to Fas-mediated apoptosis. J. Neuropathol. Exp. Neurol. 2000, 59:280-286.
56. Qi X., Hauswirth W.W., Guy J. Dual gene therapy with extracellular superoxide dismutase and catalase attenuates experimental optic neuritis. Mol. Vis. 2007, 13:1-11.
57. Ramirez-Rodriguez G., Vega-Rivera N.M., Oikawa-Sala J., Gomez-Sanchez A., Ortiz-Lopez L., Estrada-Camarena E. Melatonin synergizes with citalopram to induce antidepressant-like behavior and to promote hippocampal neurogenesis in adult mice. J. Pineal Res. 2014, 56:450-461.
58. Reddy J., Waldner H., Zhang X., Illes Z., Wucherpfennig K.W., Sobel R.A., Kuchroo V.K. Cutting edge: CD4+CD25+ regulatory T cells contribute to gender differences in susceptibility to experimental autoimmune encephalomyelitis. J. Immunol. 2005, 175:5591-5595.
59. Reiter R.J., Tan D.X., Galano A. Melatonin: exceeding expectations. Physiology (Bethesda) 2014, 29:325-333.
60. Requintina P.J., Oxenkrug G.F. Effect of luzindole and other melatonin receptor antagonists on iron- and lipopolysaccharide-induced lipid peroxidation in vitro. Ann. N. Y. Acad. Sci. 2007, 1122:289-294.
61. Ruddle N.H., Bergman C.M., McGrath K.M., Lingenheld E.G., Grunnet M.L., Padula S.J., Clark R.B. An antibody to lymphotoxin and tumor necrosis factor prevents transfer of experimental allergic encephalomyelitis. J. Exp. Med. 1990, 172:1193-1200.
62. Sandyk R. Influence of the pineal gland on the expression of experimental allergic encephalomyelitis: possible relationship to the aquisition of multiple sclerosis. Int. J. Neurosci. 1997, 90:129-133.
63. Sharief M.K., Hentges R. Association between tumor necrosis factor-alpha and disease progression in patients with multiple sclerosis. N. Engl. J. Med. 1991, 325:467-472.
64. Sharma H.S., Olsson Y., Dey P.K. Changes in blood-brain barrier and cerebral blood flow following elevation of circulating serotonin level in anesthetized rats. Brain Res. 1990, 517:215-223.
65. Shen Y., Zhang G., Liu L., Xu S. Suppressive effects of melatonin on amyloid-beta-induced glial activation in rat hippocampus. Arch. Med. Res. 2007, 38:284-290.
66. Soilu-Hanninen M., Laaksonen M., Hanninen A. Hyaluronate receptor (CD44) and integrin alpha4 (CD49d) are up-regulated on T cells during MS relapses. J. Neuroimmunol. 2005, 166:189-192.
67. Taylor A.W., Kitaichi N. The diminishment of experimental autoimmune encephalomyelitis (EAE) by neuropeptide alpha-melanocyte stimulating hormone (alpha-MSH) therapy. Brain Behav. Immun. 2008, 22:639-646.
68. Tong C.K., Chen J., Cebrian-Silla A., Mirzadeh Z., Obernier K., Guinto C.D., Tecott L.H., Garcia-Verdugo J.M., Kriegstein A., Alvarez-Buylla A. Axonal control of the adult neural stem cell niche. Cell Stem Cell 2014, 14:500-511.
69. Vigore L., Messina G., Brivio F., Fumagalli L., Rovelli F., D.I.F.G, Lissoni P. Psychoneuroendocrine modulation of regulatory T lymphocyte system: in vivo and in vitro effects of the pineal immunomodulating hormone melatonin. In Vivo 2010, 24:787-789.
70. Wildbaum G., Youssef S., Grabie N., Karin N. Neutralizing antibodies to IFN-gamma-inducing factor prevent experimental autoimmune encephalomyelitis. J. Immunol. 1998, 161:6368-6374.
71. Williams J.L., Kithcart A.P., Smith K.M., Shawler T., Cox G.M., Whitacre C.C. Memory cells specific for myelin oligodendrocyte glycoprotein (MOG) govern the transfer of experimental autoimmune encephalomyelitis. J. Neuroimmunol. 2011, 234:84-92.
72. Winkler C.W., Foster S.C., Matsumoto S.G., Preston M.A., Xing R., Bebo B.F., Banine F., Berny-Lang M.A., Itakura A., McCarty O.J., Sherman L.S. Hyaluronan anchored to activated CD44 on central nervous system vascular endothelial cells promotes lymphocyte extravasation in experimental autoimmune encephalomyelitis. J. Biol. Chem. 2012, 287:33237-33251.
73. Zamvil S.S., Steinman L. The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev. Immunol. 1990, 8:579-621.
74. Zamvil S.S., Steinman L. Diverse targets for intervention during inflammatory and neurodegenerative phases of multiple sclerosis. Neuron 2003, 38:685-688.
75. Zhang X., Koldzic D.N., Izikson L., Reddy J., Nazareno R.F., Sakaguchi S., Kuchroo V.K., Weiner H.L. IL-10 is involved in the suppression of experimental autoimmune encephalomyelitis by CD25+CD4+ regulatory T cells. Int. Immunol. 2004, 16:249-256.
76. Zhou M.O., Jiao S., Liu Z., Zhang Z.H., Mei Y.A. Luzindole, a melatonin receptor antagonist, inhibits the transient outward K+ current in rat cerebellar granule cells. Brain Res. 2003, 970:169-177.